Re-constructing our models of cellulose and primary cell wall assembly

Abstract

The cellulose microfibril has more subtlety than is commonly recognized. Details of its structure may influence how matrix polysaccharides interact with its distinctive hydrophobic and hydrophilic surfaces to form a strong yet extensible structure. Recent advances in this field include the first structures of bacterial and plant cellulose synthases and revised estimates of microfibril structure, reduced from 36 to 18 chains. New results also indicate that cellulose interactions with xyloglucan are more limited than commonly believed, whereas pectin–cellulose interactions are more prevalent. Computational results indicate that xyloglucan binds tightest to the hydrophobic surface of cellulose microfibrils. Wall extensibility may be controlled at limited regions (‘biomechanical hotspots’) where cellulose–cellulose contacts are made, potentially mediated by trace amounts of xyloglucan.

Figure 1

Potential shapes of cellulose microfibrils in cross section and impact on interactions with other wall components. Top row: potential cross sections of 36-, 24- and 18-chain microfibrils. The hydrophobic surface in each structure is indicated with the red lines. (a) Common depiction of a 36-chain microfibril cross section in a hexagonal shape. The colors represent chain mobility, with internal residues (red) more rigid than surface residues (blue). (b) According to Ding et al. [32,77], microfibrils may associate laterally via their hydrophilic surfaces. Others postulate preferential association via the hydrophobic surfaces. Two versions of a microfibril with 24-chain cross section are shown (c) in diamond shape or (d) in rectangular shape. Note how shape affects the proportion of hydrophilic and hydrophilic surfaces. (e) Busse-Wicher et al. [30*] illustrate two ways in which acetylated xylan (red residues with yellow acetyl groups) may bind to the hydrophilic surface (shown in two views) or (f) to the hydrophobic surface (likewise shown in two views). The two models in (e) and (f) make use of the 24-chain rectangular microfibril shown in (d). In (e) the xylan fits into the grooves of the hydrophilic surface of the rectangular microfibril, with the evenly-spaced acetyl groups exposed to the outside. This model would not work for the diamond-shaped structure – a striking example of how cellulose packing may affect interaction with matrix polysaccharides. Two versions of 18-chain cross sections are shown in (g) and in (h). The interaction of xyloglucan with the hydrophobic and hydrophilic surface of cellulose are illustrated in (i) and (j), based on MDS by Zhao et al. [29*]. Image credits: (a) and (b) adapted from Ding et al. [32], (i) and (j) from Zhao et al. [29], copyright Springer Verlag, used with permission. (c), (d), (g), (h) adapted from Fernandes et al. [33], copyright Proceedings of the National Academy of Sciences, used with permission. (e) and (f) from Busse-Wicher et al. [30*], copyright John Wiley & Sons, used with permission.

Figure 2

Updated models of plant CESAs and CSCs. (a) A computational model of a plant CESA catalytic domain with P-CR and CSR regions (light grey). The glucan chain (purple) is from the homologous Rhodobacter structure. The location of the transmembrane helices (TMH) is represented with grey boxes. (b) Three CESAs, encoded by three different genes, may interact to form a trimeric particle, which in turn may assemble into a hexameric rosette, depicted in (c). The glucan chains are represented in red. Image (a) is adapted from Slaubaugh et al. [37] and is courtesy of Jonathan Davis.

Figure 3

(a) Multilayered arrangement of cellulose microfibrils at the cell wall surface from onion scale, visualized by atomic force microscopy under water, without extraction or drying of the sample. (b) A close up from (a), with the microfibrils in the surface layer drawn in blue. Note that microfibrils merge into and out of regions of close contract. (c) One potential arrangement in which xyloglucan (red) serves as a monomolecular adhesive between the hydrophobic surfaces of two cellulose microfibrils (blue). Image credit: (a) is from Zhang et al. [76], (c) is from Zhao et al. [29*], both copyright Springer Verlag and used with permission.

Figure 4

Artistic depiction of the cell wall, based on the microfibril arrangement shown in Figure 3(b). Cellulose microfibrils were traced in blue. Red regions indicate potential biomechanical hotspots where two or more microfibrils merge into close contact. Highly dispersed, mobile pectins are represented in yellow (different textures to indicate different pectic domains) whereas xyloglucans are shown as green coiled structures anchored to microfibril surfaces at limited locations.